Sex difference in pathology and memory decline in rTg4510 mouse model of tauopathy

Neurobiology of Aging

Volumn 32, Issue 4, 2011, Pages 590-603

  Yue, Mei ^a   Hanna, Amanda ^a   Wilson, Judith ^a   Roder, Hanno ^a   Janus, Christopher ^a  

^a MAYO GRADUATE SCHOOL   (United States)

Author keywords

Memory impairment; Neuronal loss; Sex difference; Tau; Transgenic mice

Indexed keywords

TAU PROTEIN;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSOCIATION; BEHAVIOR DISORDER; BIOCHEMISTRY; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE MODEL; DISEASE SEVERITY; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; LEARNING DISORDER; MALE; MAZE TEST; MEMORY DISORDER; MENTAL DETERIORATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SEX DIFFERENCE; SPATIAL MEMORY; STIMULUS RESPONSE; SWIMMING; TAUOPATHY; TRANSGENE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; MALE; MAZE LEARNING; MEMORY; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; SEX CHARACTERISTICS; TAU PROTEINS; TAUOPATHIES;

EID: 79953060064     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2009.04.006     Document Type: Article

References (76)

1. Arendt T., Schindler C., Bruckner M.K., Eschrich K., Bigl V., Zedlick D., Marcova L. Plastic neuronal remodeling is impaired in patients with Alzheimer's disease carrying apolipoprotein epsilon 4 allele. J. Neurosci. 1997, 17(2):516-529.
2. Arriagada P.V., Growdon J.H., Hedley-Whyte E.T., Hyman B.T. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 1992, 42(3):631-639.
3. Arters J., Hohmann C.F., Mills J., Olaghere O., Berger-Sweeney J. Sexually dimorphic responses to neonatal basal forebrain lesions in mice. I. Behavior and neurochemistry. J. Neurobiol. 1998, 37(4):582-594.
4. Atwood C.S., Meethal S.V., Liu T., Wilson A.C., Gallego M., Smith M.A., Bowen R.L. Dysregulation of the hypothalamic-pituitary-gonadal axis with menopause and andropause promotes neurodegenerative senescence. J. Neuropathol. Exp. Neurol. 2005, 64(2):93-103.
5. Azad N.A., Al Bugami M., Loy-English I. Gender differences in dementia risk factors. Gend. Med. 2007, 4(2):120-129.
6. Banbury Conference on Genetic Background in Mice Mutant mice and neuroscience: recommendations. Neuron 1997, 19:755-759.
7. Beiko J., Lander R., Hampson E., Boon F., Cain D.P. Contribution of sex differences in the acute stress response to sex differences in water maze performance in the rat. Behav. Brain Res. 2004, 151(1-2):239-253.
8. Benice T.S., Rizk A., Kohama S., Pfankuch T., Raber J. Sex-differences in age-related cognitive decline in C57BL/6J mice associated with increased brain microtubule-associated protein 2 and synaptophysin immunoreactivity. Neuroscience 2006, 137(2):413-423.
9. Berg L., McKeel D.W., Miller J.P., Baty J., Morris J.C. Neuropathological indexes of Alzheimer's disease in demented and nondemented persons aged 80 years and older. Arch. Neurol. 1993, 50(4):349-358.
10. Berger Z., Roder H., Hanna A., Carlson A., Rangachari V., Yue M., Wszolek Z., Ashe K., Knight J., Dickson D., Andorfer C., Rosenberry T.L., Lewis J., Hutton M., Janus C. Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. J. Neurosci. 2007, 27(14):3650-3662.
11. Berger-Sweeney J., Arnold A., Gabeau D., Mills J. Sex differences in learning and memory in mice: effects of sequence of testing and cholinergic blockade. Behav. Neurosci. 1995, 109(5):859-873.
12. Bowen R.L., Smith M.A., Harris P.L., Kubat Z., Martins R.N., Castellani R.J., Perry G., Atwood C.S. Elevated luteinizing hormone expression colocalizes with neurons vulnerable to Alzheimer's disease pathology. J. Neurosci. Res. 2002, 70(3):514-518.
13. Braak H., Braak E. Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol. Aging 1997, 18(4):351-357.
14. Brody D.L., Holtzman D.M. Morris water maze search strategy analysis in PDAPP mice before and after experimental traumatic brain injury. Exp. Neurol. 2006, 197(2):330-340.
15. Buee L., Bussiere T., Buee-Scherrer V., Delacourte A., Hof P.R. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res. Brain Res. Rev. 2000, 33(1):95-130.
16. Casadesus G., Webber K.M., Atwood C.S., Pappolla M.A., Perry G., Bowen R.L., Smith M.A. Luteinizing hormone modulates cognition and amyloid-beta deposition in Alzheimer APP transgenic mice. Biochim. Biophys. Acta 2006, 1762(4):447-452.
17. Clark L.N., Poorkaj P., Wszolek Z., Geschwind D.H., Nasreddine Z.S., Miller B., Li D., Payami H., Awert F., Markopoulou K., Andreadis A., D'Souza I., Lee V.M., Reed L., Trojanowski J.Q., Zhukareva V., Bird T., Schellenberg G., Wilhelmsen K.C. Pathogenic implications of mutations in the tau gene in pallido-ponto-nigral degeneration and related neurodegenerative disorders linked to chromosome 17. Proc. Natl. Acad. Sci. U.S.A. 1998, 95(22):13103-13107.
18. Corder E.H., Saunders A.M., Pericak-Vance M.A., Roses A.D. There is a pathologic relationship between ApoE-epsilon 4 and Alzheimer's disease. Arch. Neurol. 1995, 52(7):650-651.
19. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Rimmler J.B., Locke P.A., Conneally P.M., Schmader K.E., Tanzi R.E., et al. Apolipoprotein E, survival in Alzheimer's disease patients, and the competing risks of death and Alzheimer's disease. Neurology 1995, 45(7):1323-1328.
20. Cotman C.W., Su J.H. Mechanisms of neuronal death in Alzheimer's disease. Brain Pathol. 1996, 6(4):493-506.
21. Crawley J.N., Paylor R. A proposed test battery and constellation of specific behaviural paradigms to investigate the behavioural phenotypes of transgenic and knockout mice. Horm. Behav. 1997, 31:197-211.
22. Davies R.R., Hodges J.R., Kril J.J., Patterson K., Halliday G.M., Xuereb J.H. The pathological basis of semantic dementia. Brain 2005, 128(Pt 9):1984-1995.
23. Dickson D.W. Neurodegeneration: The Molecular Pathology of Dementia and Movement Disorders 2003, ISN Neuropath Press, Basel.
24. Eichenbaum H. Learning from LTP: a comment on recent attempts to identify cellular and molecular mechanisms of memory. Learn. Mem. 1996, 3:61-73.
25. Eriksen J.L., Janus C.G. Plaques, tangles, and memory loss in mouse models of neurodegeneration. Behav. Genet. 2006, 37(1):79-100.
26. Erten-Lyons D., Woltjer R.L., Dodge H., Nixon R., Vorobik R., Calvert J.F., Leahy M., Montine T., Kaye J. Factors associated with resistance to dementia despite high Alzheimer disease pathology. Neurology 2009, 72(4):354-360.
27. Farrer L.A., Cupples L.A., Haines J.L., Hyman B., Kukull W.A., Mayeux R., Myers R.H., Pericak-Vance M.A., Risch N., van Duijn C.M. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. APOE and Alzheimer Disease Meta Analysis Consortium. JAMA 1997, 278(16):1349-1356.
28. Fleisher A., Grundman M., Jack C.R., Petersen R.C., Taylor C., Kim H.T., Schiller D.H., Bagwell V., Sencakova D., Weiner M.F., DeCarli C., DeKosky S.T., van Dyck C.H., Thal L.J. Sex, apolipoprotein E epsilon 4 status, and hippocampal volume in mild cognitive impairment. Arch. Neurol. 2005, 62(6):953-957.
29. Frick K.M., Burlingame L.A., Arters J.A., Berger-Sweeney J. Reference memory, anxiety and estrous cyclicity in C57BL/6NIA mice are affected by age and sex. Neuroscience 2000, 95(1):293-307.
30. Frye C.A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol. Behav. 1995, 57(1):5-14.
31. Frye C.A., Sturgis J.D. Neurosteroids affect spatial/reference, working, and long-term memory of female rats. Neurobiol. Learn. Mem. 1995, 64(1):83-96.
32. Gass P., Wolfer D.P., Balschun D., Rudolph D., Frey U., Lipp H.P., Schütz G. Deficits in memory tasks of mice with CREB mutations depend on gene dosage. Learn. Mem. 1998, 5:274-288.
33. Goedert M., Jakes R. Mutations causing neurodegenerative tauopathies. Biochim. Biophys. Acta 2005, 1739(2-3):240-250.
34. Gossen M., Bujard H. Efficacy of tetracycline-controlled gene expression is influenced by cell type: commentary. Biotechniques 1995, 19(2):213-216. discussion 216-217.
35. Greenberg S.G., Davies P. A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc. Natl. Acad. Sci. U.S.A. 1990, 87(15):5827-5831.
36. Hirata-Fukae C., Li H.F., Hoe H.S., Gray A.J., Minami S.S., Hamada K., Niikura T., Hua F., Tsukagoshi-Nagai H., Horikoshi-Sakuraba Y., Mughal M., Rebeck G.W., LaFerla F.M., Mattson M.P., Iwata N., Saido T.C., Klein W.L., Duff K.E., Aisen P.S., Matsuoka Y. Females exhibit more extensive amyloid, but not tau, pathology in an Alzheimer transgenic model. Brain Res. 2008, 1216:92-103.
37. Hutton M., Lendon C.L., Rizzu P., Baker M., Froelich S., Houlden H., Pickering-Brown S., Chakraverty S., Isaacs A., Grover A., Hackett J., Adamson J., Lincoln S., Dickson D., Davies P., Petersen R.C., Stevens M., de Graaff E., Wauters E., van Baren J., Hillebrand M., Joosse M., Kwon J.M., Nowotny P., Che L.K., Norton J., Morris J.C., Reed L.A., Trojanowski J., Basun H., Lannfelt L., Neystat M., Fahn S., Dark F., Tannenberg T., Dodd P.R., Hayward N., Kwok J.B., Schofield P.R., Andreadis A., Snowden J., Craufurd D., Neary D., Owen F., Oostra B.A., Hardy J., Goate A., van Swieten J., Mann D., Lynch T., Heutink P. Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998, 393(6686):702-705.
38. Imwalle D.B., Bateman H.L., Wills A., Honda S., Harada N., Rissman E.F. Impairment of spatial learning by estradiol treatment in female mice is attenuated by estradiol exposure during development. Horm. Behav. 2006, 50(5):693-698.
39. Iqbal K., Alonso Adel C., Chen S., Chohan M.O., El-Akkad E., Gong C.X., Khatoon S., Li B., Liu F., Rahman A., Tanimukai H., Grundke-Iqbal I. Tau pathology in Alzheimer disease and other tauopathies. Biochim. Biophys. Acta 2005, 1739(2-3):198-210.
40. Janus C. Search strategies used by APP transgenic mice during spatial navigation in the Morris water maze. Learn. Mem. 2004, 11:337-346.
41. Janus C. Contitionally inducible tau mice-designing a better mouse model of neurodegenerative diseases. Genes Brain Behav. 2008, 7(Suppl. 1):12-28.
42. Kavaliers M., Ossenkopp K.P., Prato F.S., Innes D.G., Galea L.A., Kinsella D.M., Perrot-Sinal T.S. Spatial learning in deer mice: sex differences and the effects of endogenous opioids and 60Hz magnetic fields. J. Comp. Physiol. [A] 1996, 179(5):715-724.
43. Lee V.M., Goedert M., Trojanowski J.Q. Neurodegenerative tauopathies. Annu. Rev. Neurosci. 2001, 24:1121-1159.
44. Lewis J., McGowan E., Rockwood J., Melrose H., Nacharaju P., Van Slegtenhorst M., Gwinn-Hardy K., Paul Murphy M., Baker M., Yu X., Duff K., Hardy J., Corral A., Lin W.L., Yen S.H., Dickson D.W., Davies P., Hutton M. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat. Genet. 2000, 25(4):402-405.
45. Lewis J., Dickson D.W., Lin W.L., Chisholm L., Corral A., Jones G., Yen S.H., Sahara N., Skipper L., Yager D., Eckman C., Hardy J., Hutton M., McGowan E. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001, 293(5534):1487-1491.
46. Lipp H.P., Wolfer D.P. Genetically modified mice and cognition. Curr. Opin. Neurobiol. 1998, 8:272-280.
47. Markowska A.L. Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J. Neurosci. 1999, 19(18):8122-8133.
48. Mayford M., Bach M.E., Huang Y.Y., Wang L., Hawkins R.D., Kandel E.R. Control of memory formation through regulated expression of a CaMKII transgene. Science 1996, 274(5293):1678-1683.
49. Morris R. Developments of a water-maze procedure for studying spatal learning in the rat. J. Neurosci. Methods 1984, 11:47-60.
50. Morris R.G.M., Garrund P., Rawlings J., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
51. Perrot-Sinal T.S., Kostenuik M.A., Ossenkopp K.P., Kavaliers M. Sex differences in performance in the Morris water maze and the effects of initial nonstationary hidden platform training. Behav. Neurosci. 1996, 110(6):1309-1320.
52. Raber J., Wong D., Buttini M., Orth M., Bellosta S., Pitas R.E., Mahley R.W., Mucke L. Isoform-specific effects of human apolipoprotein E on brain function revealed in ApoE knockout mice: increased susceptibility of females. Proc. Natl. Acad. Sci. U.S.A. 1998, 95(18):10914-10919.
53. Raber J., Wong D., Yu G.Q., Buttini M., Mahley R.W., Pitas R.E., Mucke L. Apolipoprotein E and cognitive performance. Nature 2000, 404(6776):352-354.
54. Raber J., Bongers G., LeFevour A., Buttini M., Mucke L. Androgens protect against apolipoprotein E4-induced cognitive deficits. J. Neurosci. 2002, 22(12):5204-5209.
55. Raber J. Androgens, apoE, and Alzheimer's disease. Sci. Aging Knowledge Environ. 2004, 2004(11):re2.
56. Ramsden M., Kotilinek L., Forster C., Paulson J., McGowan E., SantaCruz K., Guimaraes A., Yue M., Lewis J., Carlson G., Hutton M., Ashe K.H. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J. Neurosci. 2005, 25(46):10637-10647.
57. Rhodin J.A., Thomas T. A vascular connection to Alzheimer's disease. Microcirculation 2001, 8(4):207-220.
58. Ribé E.M., Perez M., Puig B., Gich I., Lim F., Cuadrado M., Sesma T., Catena S., Sanchez B., Nieto M., Gomez-Ramos P., Moran M.A., Cabodevilla F., Samaranch L., Ortiz L., Perez A., Ferrer I., Avila J., Gomez-Isla T. Accelerated amyloid deposition, neurofibrillary degeneration and neuronal loss in double mutant APP/tau transgenic mice. Neurobiol. Dis. 2005, 20(3):814-822.
59. Santa Cruz K., Lewis J., Spires T., Paulson J., Kotilinek L., Ingelsson M., Guimaraes A., DeTure M., Ramsden M., McGowan E., Forster C., Yue M., Orne J., Janus C., Mariash A., Kuskowski M., Hyman B., Hutton M., Ashe K.H. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005, 309(5733):476-481.
60. Schenk F. Development of place navigation in rats from weaning to puberty. Behav. Neural Biol. 1985, 43(1):69-85.
61. Schindowski K., Bretteville A., Leroy K., Begard S., Brion J.P., Hamdane M., Buee L. Alzheimer's disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. Am. J. Pathol. 2006, 169(2):599-616.
62. Selkoe D.J. Alzheimer's disease: genotypes, phenotypes, and treatments. Science 1997, 275:630-631.
63. Sergeant N., Delacourte A., Buee L. Tau protein as a differential biomarker of tauopathies. Biochim. Biophys. Acta 2005, 1739(2-3):179-197.
64. Spires T.L., Meyer-Luehmann M., Stern E.A., McLean P.J., Skoch J., Nguyen P.T., Bacskai B.J., Hyman B.T. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J. Neurosci. 2005, 25(31):7278-7287.
65. Spires T.L., Orne J.D., SantaCruz K., Pitstick R., Carlson G.A., Ashe K.H., Hyman B.T. Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am. J. Pathol. 2006, 168(5):1598-1607.
66. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 1992, 99(2):195-231.
67. Stevens J. Intermediate Statistics: A Modern Approach 1990, Lawrence Erlbaum Associates, Inc., Publishers, Hillsdale, NJ.
68. Terry R.D. Alzheimer's disease and the aging brain. J. Geriatr. Psychiatry Neurol. 2006, 19(3):125-128.
69. Terwel D., Lasrado R., Snauwaert J., Vandeweert E., Van Haesendonck C., Borghgraef P., Van Leuven F. Changed conformation of mutant Tau-P301L underlies the moribund tauopathy, absent in progressive, nonlethal axonopathy of Tau-4R/2N transgenic mice. J. Biol. Chem. 2005, 280(5):3963-3973.
70. van Meer P., Acevedo S., Raber J. Impairments in spatial memory retention of GFAP-apoE4 female mice. Behav. Brain Res. 2007, 176(2):372-375.
71. Wahlsten D., Cooper S.F., Crabbe J.C. Different rankings of inbred mouse strains on the Morris maze and a refined 4-arm water escape task. Behav. Brain Res. 2005, 165(1):36-51.
72. Warren S.G., Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behav. Neurosci. 1997, 111(2):259-266.
73. Webber K.M., Bowen R., Casadesus G., Perry G., Atwood C.S., Smith M.A. Gonadotropins and Alzheimer's disease: the link between estrogen replacement therapy and neuroprotection. Acta Neurobiol. Exp. (Wars) 2004, 64(1):113-118.
74. Wehner J.M., Sleight S., Upchurch M. Hippocampal protein kinase C activity is reduced in poor spatial learners. Brain Res. 1990, 523:181-187.
75. Williams M.M., Xiong C., Morris J.C., Galvin J.E. Survival and mortality differences between dementia with Lewy bodies vs Alzheimer disease. Neurology 2006, 67(11):1935-1941.
76. Wolfer D.P., Lipp H.P. Dissecting the behaviour of transgenic mice: is it the mutation, the genetic background, or the environment. Exp. Physiol. 2000, 85(6):627-634.